Blockade of self-reactive IgM significantly reduces injury in a murine model of acute myocardial infarction

Cardiovascular Research

Volumn 87, Issue 4, 2010, Pages 618-627

  Haas, Michael S ^a   Alicot, Elisabeth M ^a,b   Schuerpf, Franziska ^a   Chiu, Isaac ^b   Li, Jinan ^c   Moore, Francis D ^d,e   Carroll, Michael C ^b  

^a DecImmune Therapeutics   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c UMEÅ UNIVERSITY   (Sweden)

^d HARVARD MEDICAL SCHOOL   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Antibodies; Lymphocytes; Myocardial infarction; Peptides; Reperfusion

Indexed keywords

COLLAGEN; IMMUNOGLOBULIN F(AB')2 FRAGMENT; IMMUNOGLOBULIN M; MONOCLONAL ANTIBODY; MYOSIN HEAVY CHAIN; MYOSIN HEAVY CHAIN 2; TROPONIN I; UNCLASSIFIED DRUG;

ACUTE HEART INFARCTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; HEART INFARCTION SIZE; ISCHEMIA; MONOCYTE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; REPERFUSION INJURY;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; COLLAGEN; DISEASE MODELS, ANIMAL; EPITOPES; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOGLOBULIN M; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR MIMICRY; MONOCYTES; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; MYOSIN HEAVY CHAINS; NEUTROPHIL INFILTRATION; PEPTIDES; TIME FACTORS; TROPONIN I;

EID: 77955893788     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvq141     Document Type: Article

References (45)

1. Kumar V, Abbas AK, Fausto N, Aster JC. Robbins and Contran Pathologic Basis of Disease, Professional Edition. 8th ed. Philadelphia, PA: Saunders Elsevier; 2010.
2. Wu B, Ootani A, Iwakiri R, Fujise T, Tsunada S, Toda S et al. Ischemic preconditioning attenuates ischemia-reperfusion-induced mucosal apoptosis by inhibiting the mitochondria-dependent pathway in rat small intestine. Am J Physiol Gastrointest Liver Physiol 2004;286:G580-G587.
3. Thiemermann C, Bowes J, Myint FP, Vane JR. Inhibition of the activity of poly(ADP ribose) synthetase reduces ischemia-reperfusion injury in the heart and skeletal muscle. Proc Natl Acad Sci USA 1997;94:679-683.
4. Piot C, Croisille P, Staat P, Thibault H, Rioufol G, Mewton N et al. Effect of cyclos-porine on reperfusion injury in acute myocardial infarction. N Engl J Med 2008;359: 473-481.
5. Inagaki K, Chen L, Ikeno F, Lee FH, Imahashi K, Bouley DM et al. Inhibition of delta-protein kinase C protects against reperfusion injury of the ischemic heart in vivo. Circulation 2003;108:2304-2307.
6. Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 2008;88:581-609.
7. Li C, Jackson R. Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol 2002;282:C227-C241.
8. Zhang M, Alicot EM, Chiu I, Li J, Verna N, Vorup-Jensen T et al. Identification of the target self-antigens in reperfusion injury. J Exp Med 2006;203:141-152.
9. Hart ML, Ceonzo KA, Shaffer LA, Takahashi K, Rother RP, Reenstra WR et al. Gastrointestinal ischemia-reperfusion injury is lectin complement pathway dependent without involving C1q. J Immunol 2005;174:6373-6380.
10. Busche MN, Pavlov V, Takahashi K, Stahl GL. Myocardial ischemia and reperfusion injury is dependent on both IgM and mannose-binding lectin. Am J Physiol Heart Circ Physiol 2009;297:H1853-H1859.
11. Zhang M, Takahashi K, Alicot EM, Vorup-Jensen T, Kessler B, Thiel S et al. Activation of the lectin pathway by natural IgM in a model of ischemia/reperfusion injury. J Immunol 2006;177:4727-4734.
12. Pepys MB, Hirschfield GM, Tennent GA, Gallimore JR, Kahan MC, Bellotti V et al. Targeting C-reactive protein for the treatment of cardiovascular disease. Nature 2006; 440:1217-1221.
13. Hill JH, Ward PA. The phlogistic role of C3 leukotactic fragments in myocardial infarcts of rats. J Exp Med 1971;133:885-900.
14. Weisman HF, Bartow T, Leppo MK, Marsh HC, Carson GR, Concino MF et al. Soluble human complement receptor type I: in vivo inhibitor of complement suppressing post-ischemic myocardial inflammation and necrosis. Science 1990;249:146-151.
15. Huang J, Kim L, Mealey R, Marsh H, Zhang Y, Tenner A et al. Neuronal protection in stroke by an sLex-glycosylated complement inhibitory protein. Science 1999;285: 595-599.
16. Lindsay TF, Hill J, Ortiz F, Rudolph A, Valeri CR, Hechtman HB et al. Blockade of complement activation prevents local and pulmonary albumin leak after lower torso ischemia-reperfusion. Ann Surg 1992;216:677-683.
17. Hill J, Lindsay TF, Ortiz F, Yeh CG, Hechtman HB, Moore FD Jr. Soluble complement receptor type 1 ameliorates the local and remote organ injury after intestinal ischemia-reperfusion in the rat. J Immunol 1992;149:1723-1728.
18. Reid RR, Woodcock S, Shimabukuro-Vornhagen A, Austen WG Jr, Kobzik L, Zhang M et al. Functional activity of natural antibody is altered in Cr2-deficient mice. J Immunol 2002;169:5433-5440.
19. Weiser M, Williams J, Moore F, Kobzik L, Ma M, Hechtman H et al. Reperfusion injury of ischemic skeletal muscle is mediated by natural antibody and complement. J Exp Med 1996;183:2343-2348.
20. Williams JP, Moore FD, Kobzik L, Carroll MC, Hechtman HB. Intestinal reperfusion injury is mediated by IgM and complement. J Appl Physiol 1999;86:938-942.
21. Zhang M, Austen WG Jr, Chiu I, Alicot EM, Hung R, Ma M et al. Identification of a specific self-reactive IgM antibody that initiates intestinal ischemia/reperfusion injury. Proc Natl Acad Sci USA 2004;101:3886-3891.
22. Chan RK, Verna N, Afnan J, Zhang M, Ibrahim S, Carroll MC et al. Attenuation of skeletal muscle reperfusion injury with intravenous 12 amino acid peptides that bind to pathogenic IgM. Surgery 2006;139:236-243.
23. Michael LH, Entman ML, Hartley CJ, Youker KA, Zhu J, Hall SR et al. Myocardial ischemia and reperfusion: a murine model. Am J Physiol 1995;269:H2147-H2154.
24. Leung H. Using photoshop for measurement and analysis. Bull Micro Soc Canada 2003; 31:19-22.
25. Arnold JN, Wormald MR, Suter DM, Radcliffe CM, Harvey DJ, Dwek RA et al. Human serum IgM glycosylation: identification of glycoforms that can bind to mannan-binding lectin. J Biol Chem 2005;280:29080-29087.
26. Zhang M, Michael L, Grosjean S, Kelly R, Carroll M, Entman M. The role of natural IgM in myocardial ischemia-reperfusion injury. J Mol Cell Cardiol 2006;41:62-67.
27. Hirsch S, Gordon S. Polymorphic expression of a neutrophil differentiation antigen revealed by monoclonal antibody 7/4. Immunogenetics 1983;18:229-239.
28. Zhang M, Alicot EM, Carroll MC. Human natural IgM can induce ischemia/reperfusion injury in a murine intestinal model. Mol Immunol 2008;45:4036-4039.
29. Lloyd-Jones D, Adams RJ, Todd M, Ford E, Furie K, Gillespie C et al. Heart disease and stroke statistics 2010 update: a report from the American Heart Association. Circulation 2010;121:e46-e215.
30. Braunwald E, Kloner RA. Myocardial reperfusion: a double-edged sword? J Clin Invest 1985;76:1713-1719.
31. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med 2007;357: 1121-1135.
32. Chan RK, Ibrahim SI, Takahashi K, Kwon E, McCormack M, Ezekowitz A et al. The differing roles of the classical and mannose-binding lectin complement pathways in the events following skeletal muscle ischemia-reperfusion. J Immunol 2006;177:8080-8085.
33. Johnson AR, Hugli TE, Muller-Eberhard HJ. Release of histamine from rat mast cells by the complement peptides C3a and C5a. Immunology 1975;28:1067-1080.
34. el-Lati SG, Dahinden CA, Church MK. Complement peptides C3a-and C5a-induced mediator release from dissociated human skin mast cells. J Invest Dermatol 1994;102: 803-806.
35. Lim HW, He D, Esquenazi-Behar S, Yancey KB, Soter NA. C5a, cutaneous mast cells, and inflammation: in vitro and in vivo studies in a murine model. J Invest Dermatol 1991;97:305-311.
36. Bolli R, Becker L, Gross G, Mentzer R Jr, Balshaw D, Lathrop DA. Myocardial protection at a crossroads: the need for translation into clinical therapy. Circ Res 2004;95: 125-134.
37. De Vries B, Matthijsen RA, Wolfs TG, Van Bijnen AA, Heeringa P, Buurman WA. Inhibition of complement factor C5 protects against renal ischemia-reperfusion injury: inhibition of late apoptosis and inflammation. Transplantation 2003;75:375-382. (Pubitemid 36222966)
38. Lefer DJ, Shandelya SM, Serrano CV Jr, Becker LC, Kuppusamy P, Zweier JL. Cardi-oprotective actions of a monoclonal antibody against CD-18 in myocardial ischemia-reperfusion injury. Circulation 1993;88:1779-1787.
39. Hansen PR. Role of neutrophils in myocardial ischemia and reperfusion. Circulation 1995;91:1872-1885.
40. Testa L, Van Gaal WJ, Bhindi R, Biondi-Zoccai GG, Abbate A, Agostoni P et al. Pex-elizumab in ischemic heart disease: a systematic review and meta-analysis on 15,196 patients. J Thorac Cardiovasc Surg 2008;136:884-893.
41. Faxon DP, Gibbons RJ, Chronos NA, Gurbel PA, Sheehan F. The effect of blockade of the CD11/CD18 integrin receptor on infarct size in patients with acute myocardial infarction treated with direct angioplasty: the results of the HALT-MI study. J Am Coll Cardiol 2002;40:1199-1204.
42. Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo JL et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 2007;204:3037-3047.
43. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009;325:612-616.
44. Frangogiannis NG. The mechanistic basis of infarct healing. Antioxid Redox Sign 2006;8: 1907-1939.
45. Hausenloy DJ, Yellon DM. Time to take myocardial reperfusion injury seriously. N Engl J Med 2008;359:518.